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Journal of Wildlife Diseases, 41(4), 2005, pp. 768-774
© Wildlife Disease Association  2005
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ASSESSMENT OF NEWCASTLE DISEASE VACCINATION OF HOUBARA BUSTARD BREEDERS (CHLAMYDOTIS UNDULATA UNDULATA)

Charles Facon1,2, Jean-Luc Guerin2 and Frédéric Lacroix1,3

1 Emirates Center for Wildlife Propagation, Province de Boulemane—B.P. 47, 33250 Missour, Royaume du Maroc
2 ENV Toulouse, Chemin des Capelles, 31076 Toulouse cedex, France
3 Corresponding author (email: flacroixecwp{at}net.ma)


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
ABSTRACT:   The houbara bustard (Chlamydotis undulata undulata) is endangered in North Africa. Through a captive-breeding program established in Morocco by The Emirates Center for Wildlife Propagation, wild populations are being supplemented by the releasing of captive-reared birds. Newcastle disease, which is caused by Newcastle disease virus (NDV; Avian paramyxovirus type 1), can infect houbara bustards and is a significant threat through contact with backyard poultry and possibly wild birds. Three vaccination schedules for Newcastle disease were evaluated by serologic monitoring to assess the efficiency and safety of various types of vaccines (live vs. inactivated), vaccine strains (Hitchner B1 and Clone 30), and administration routes (intranasal vs. injection). We evaluated antibody titers in 211 adult houbara bustards for 10 mo. Antibody titers to NDV in both sera and egg yolks were monitored by hemagglutination inhibition test. The inactivated vaccine provided a high, homogeneous, and durable serologic response in breeders; titers were higher than log2 11 after 4 wk and remained higher than log2 7 after 10 mo. The response to the two live vaccines was similar, and antibody titers did not exceed log2 6 at sero-conversion. Maternally derived antibodies were efficiently transmitted in vitellus, further confirming that offspring of females hyperimmunized with the inactivated vaccine received high titers of maternal antibodies.
  Key words:  Avian paramyxovirus type 1, Chlamydotis undulata undulata, houbara bustard, maternal antibodies, Newcastle disease, Newcastle disease virus, vaccination.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
The houbara bustard Chlamydotis undulata undulate is an endangered species living in North Africa. It is a sedentary bird living in arid environments, where it rains less than 200 mm annually (Goriup, 1983). The Emirates Center for Wildlife Propagation (ECWP) sustains wild populations by releasing captive-produced bustards (Lacroix, 2003). The Emirates Center for Wildlife Propagation is situated in Morocco, where Newcastle disease (ND) is routinely diagnosed in both commercial and backyard poultry, despite the absence of officially reported ND cases since 1986 (Bell, 1984; OIE, 2003). Macqueen’s bustard (Chlamydotis macqueeni) also is susceptible to ND (Bailey et al., 1996a, b, 1997).

Newcastle disease is caused by Newcastle disease virus (NDV; avian paramyxovirus-1), tentatively included in the genus Rubulavirus within the Paramyxoviridae (Van Regenmortel et al., 2000); NDV infection has been documented in many wild and migratory bird species (Kaleta and Baldauf, 1988; Takakuwa et al., 1998). Transmission occurs either directly (through contact with infected birds or pseudo-vertically through eggshell contamination) or indirectly (via respiratory aerosol, fecal contamination of food and water). Clinical signs are polymorphic, depending on the tropism and virulence of the virus strain, target species, and vaccinal immunity (Alexander, 2003). The most pathogenic pathotypes, referred to as "velogenic viscerotropic," are routinely isolated in Morocco (Bell, 1986; Bell and Mouahid, 1987; Facon, 2002). These strains are typically associated with hemorrhagic intestinal lesions. This classification should be considered with caution, however, as variation in clinical response can occur between viruses within the same pathotype (Alexander, 2000).

Although NDV vaccines are not specifically produced for houbara bustard, commercial vaccines are licensed in most countries for use in domestic chickens and turkeys. Prior to this study, NDV vaccination of bustards at the ECWP in Morocco was based on a live Hitchner B1 vaccine, administered biannually by nasal instillation. While both live Hitchner B1 and Clone 30 (derived from the strain La Sota) are innocuous when administered to poultry species, dramatic differences in their efficacy have been reported (Alexander, 2000).

Protection against an experimental challenge with NDV cannot be correlated with the serologic response to vaccination with live vaccines administered through mucosal (mostly intranasal) routes; protection against an intranasal challenge can occur in cases in which the serologic response is poor. In contrast, the immune response following a parenteral vaccination, using an inactivated vaccine, is mostly humoral and is highly protective against an intramuscular challenge (Alexander, 2003). In the same way, protection of the day-old chick is strictly conferred through maternally derived antibodies, and serologic monitoring of breeders provides a reliable indication of NDV immunity in day-old chicks (Meulemans, 1988).

Currently, different breeding centers for houbara bustards are not using uniform NDV vaccination protocols (Bailey et al., 2000). Since the extent of captive breeding of this species is expanding in North Africa and the Middle East, a rational assessment of vaccination against NDV is required. Here we report a comprehensive study of NDV vaccination strategies applied to houbara bustard breeders. Three vaccination schedules for ND were evaluated by serologic monitoring of both sera and egg yolks to assess the efficiency and safety of various types of vaccines (live and inactivated), vaccine strains (Hitchner B1 vs. Clone 30), and administration routes (intranasal and injection).


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Birds

Houbara bustards (n=180) were divided into three groups of 60 birds, each consisting of an equal number of males and females. Males and females hatched in 2001 are designated as groups A and B, respectively (Table 1Go). All of the bustards were hatched in 2001 and maintained in ECWP facilities; each bird was housed separately. In the same manner, 31 females hatched in 2000 and maintained in ECWP facilities were included in the study and comprised group C (Table 1Go).


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  		TABLE 1. Experimental design of the vaccine trials. For each population of birds (A, B, and C), three groups were sampled and submitted to a vaccine program.

 
Vaccines

Three vaccines were used, including a Hitchner B1 live vaccine (Hitchner B1 Nobilis®, Intervet, Boxmeer, The Netherlands) applied by nasal instillation after reconstitution in NaCl solution buffer; a Clone 30 live vaccine (Clone 30 Nobilis®, Intervet) applied by nasal instillation after reconstitution in NaCl solution buffer; and an inactivated Clone 30 water-in-oil adjuvanted vaccine (Newcavac Nobilis®, Intervet) injected subcutaneously (SC) at the dorsal base of the neck. These three vaccines are referred to as vaccine groups 1, 2, and 3, respectively (Table 1Go).

Vaccination schedules

All birds received two doses of vaccine at 1 and 2 mo of age using a double dose of Hitchner B1 vaccine. Females hatched in 2000 received a booster dose every 6 mo with the same vaccine. A booster vaccination was administered as follows: 1) The live Hitchner B1 vaccine was applied to vaccine group 1, consisting of 30 males (group A1), 30 females (group 1B) hatched in 2001, and 15 females hatched in 2000 (group C1); 2) The live Clone 30 vaccine was applied to vaccine group 2, consisting of 30 males (group A2) and 30 females (group B2) hatched in 2001; and 3) The inactivated vaccine was applied to vaccine group 3, consisting of 30 males (group A3), 30 females (group B3) hatched in 2001, and 16 females hatched in 2000 (group C3).

Clinical response to vaccination

Following vaccination, birds were monitored daily for 10 days for changes in behavior, food intake, and weight and were subjected to a complete clinical examination. The safety of live Clone 30 and inactivated vaccine had been previously determined in a trial on 18 bustards conducted before this study.

Blood sampling and serology

For collection of sera, birds were bled every 4 wk after booster vaccination for a period of 4 mo at week 9 (T1), week 13 (T2), week 17 (T3), and week 21 (T4), respectively. In addition, serum was collected from males at week 40 (T5) and week 49 (T6). Blood was collected into silicone tubes (evacuated blood collection tubes, Terumo Europe, Belgium), by venepuncture of the right brachial vein. Blood was allowed to clot at 4 C and was then centrifuged for 10 min at 1,000 x G. Sera were stored at – 20 C and sent to the Laboratoire de Développement et d’Analyses des Côtes d’Armor (LDA22) in France. Antibody titers to NDV were determined using the hemagglutination inhibition test (HI), which is conventionally used to detect and quantify NDV antibodies (Allan et al., 1978; Piela et al, 1984; OIE, 2000).

Collection of egg yolks and immunoglobulin Y purification

For all females, the first egg of the laying period was not inseminated and was devoted to extraction of immunoglobulin Y (IgY) and subsequent HI NDV assay. Immunoglobulin Y was purified using a commercial kit (Eggcellent Chicken IgY Purification Kit, Pierce, Rockford, Illinois, USA). Aliquots of purified proteins were frozen at –20 C and then sent to the LDA 22 for serology.

Statistical analysis

Data were analyzed using the Student’s independent t-test. Systat software (SPSS, Inc. Chicago, Illinois, USA) was used for all statistical calculations. Statistical significance was set to P=0.05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Throughout the trials, no changes in behavior, food intake, or reduced weight gain were observed, and birds vaccinated with live Clone 30 showed no nasal discharge or dyspnea. After the SC injection of inactivated vaccine, two birds showed an erythema of less than 1 cm in diameter for 3–4 days. Body weight was monitored at each sampling period, and mean weights for females and males were 1,224±119 g and 1,722±172 g, respectively. No clinical signs suggestive of ND were observed in birds during the experiment.

Because our experimental conditions did not allow the inclusion of a nonvaccinated group, results were analyzed in reference to the standard vaccination schedule routinely used in ECWP, using HB1 live vaccine (groups A1, B1, and C1, respectively). The serologic responses to the three vaccines were compared for male and female breeders born in 2001 and for both groups; responses to HB1 (vaccine groups A1 and B1) and Clone 30 (vaccine groups A2 and B2) were low and mostly equivalent (Figs. 1Go, 2Go). Antibody titers reached log2 5.5±2.8 for both A1 and B1 groups and log2 5.8±3.3 for combined A2 and B2 groups. In contrast, the inactivated vaccine induced a higher serologic response, with less variation in titer observed among individual birds; HI titers were elevated to log2 11.4±1.2 at T1 and were still high (log2 9.6±1.0) at T4 (Figs. 1Go, 2Go).


Figure 1
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  		FIGURE 1. Serologic response to booster vaccination of male houbara bustards (group A), during 44 wk. Newcastle disease virus antibody hemagglutination (HI) titers are expressed in log2 (±SD).

 

Figure 2
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  		FIGURE 2. Serologic response to booster vaccination of female houbara bustards, born in 2001 (group B), during 16 wk. Newcastle disease virus antibody hemagglutination (HI) titers are expressed in log2 (±SD).

 
Females hatched in 2000 (group C) showed higher serologic titers following boosting, since they had received two additional HB1 vaccinations. Compared to females hatched in 2001, seroconversion titers after HB1 boosting were significantly increased (P=0.06), while the two groups of birds (3B and 3C) vaccinated using the inactivated vaccine showed similar serologic results (P=0.34) (Fig. 3Go). Antibody titers associated with the inactivated vaccine were not only higher but were also more consistent, as indicated by standard deviation shown in Figures 1Go and 2Go.


Figure 3
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  		FIGURE 3. Hemagglutination (HI) Newcastle disease virus antibody titers, log2 (±SD), of houbara bustards females: comparison of HI response between generation 2000 and generation 2001, during 16 wk.

 
Transmission of maternal antibody through eggs was determined through HI titration of egg yolks (Fig. 4Go). Mean HI titers in egg yolk after vaccination with inactivated vaccine, HB1 and Clone 30, were 8.4 (eggs from C3, n=9), 10.1 (eggs from B3, n=9); 5.7 (eggs from C1, n=7), 3.1 (eggs from B1, n=7); and 4.0 (eggs from B2, n=5). The ratios between egg yolk and serum HI titers were 0.85±0.14, 0.99±0.09, 0.95±0.11, 0.76±0.35, and 0.71±0.40, respectively, for these groups.


Figure 4
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  		FIGURE 4. Hemagglutination (HI) Newcastle disease virus antibody titers, log2 (±SD), in egg yolks of females hatched in 2001 (group B) and in 2000 (group C).

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
The aim of this work was to define an optimal vaccination schedule for houbara bustard breeders. In our hands, the inactivated oil–adjuvanted NDV induced a high and persistent antibody response, regardless of sex, age, or previous immune status. Similar results have been previously indicated, but these data were obtained from as few as six birds (Bailey et al., 1998a). In chickens, NDV HI titers greater to or equal than log2 5 units are considered to be protective against a field challenge (Phillips, 1973). In our vaccination experiment, HI titers reached log2 11.4 at seroconversion, and at 44 wk after the booster vaccine, titers still averaged log2 7.5. Protective titers were maintained for up to 9 mo, as has been reported elsewhere for gallinaceous birds (Eidson et al., 1980; Gerlach, 1994). Our results indicate that protection against NDV was not produced with our previous vaccination schedule using Hitchner B1, since titers never exceeded log2 5 units following seroconversion. The live vaccines (Hitchner B1 and Clone 30) induced similar serologic responses (groups 1 and 2). However, the efficacy of Clone 30 is uncertain, since clinical protection associated with this vaccine has not been thoroughly evaluated through challenge experiments.

Using the inactivated vaccine, antibody titers were not only higher than with Hitchner B1 and Clone 30, but they remained fairly consistent through the laying period. In a previous study (Bailey et al., 1998a), a dose of 1.0 ml/kg was recommended for inactivated vaccine in male bustards. However, houbara bustards show a significant sexual dimorphism; males were 41% heavier than females in our experiment. In our trial, performed on 30 males and 30 females, no difference in HI response was detected between males and females after administration of the same dose of 0.5 ml. One can hypothesize that the antigen load is so high (greater than 50 units of protective dose50 for chicken) that no difference in HI response could be observed between males and females. These results indicate that the recommended dose of 0.5 ml inactivated vaccine per bird is sufficient for both male and female houbara bustard vaccination.

Because of the endangered status of houbara bustards, infectious challenges are not possible. The level of protection, therefore, represented a value extrapolated from data obtained from chickens, in which HI tests are routinely used to evaluate NDV vaccination results as an alternative to viral challenge (Allan et al., 1978). This assay (HI) is more accurate for assessment of field protection than are test results from enzyme-linked immunosorbent assay test kits (Alexander, 2003).

Hemagglutination inhibition titers in egg yolks were consistent with maternal antibody HI titers for all three vaccines, but higher antibody titers were detected in eggs from females immunized with the inactivated vaccine. The ratio between serum and egg yolk HI titers was also assessed and showed no significant differences between vaccines. The absorption of NDV antibodies from eggs to chicks is now well documented, and in gallinaceous birds, antibody titers of day-old chicks are equivalent to those of their hyperimmunized parents (Van Eck, 1990) and those resulting from parallel immunization of hens (Eidson et al., 1982). Yeo et al. (2003) demonstrated a good correlation between yolk- and chick-HI antibody titers, as well as between yolks and hens. Finally, absorption of maternal NDV antibodies from chicks of kori bustards (Ardeotis kori) has been reported (Bailey et al., 1998b).

Because initial NDV replication occurs in the respiratory and/or digestive tracts, one could theorize that vaccination should be focused on induction of mucosal immune response (Russel, 1993). However, maternal antibody transfer and subsequent protection of day-old chicks is a critical issue for NDV control. Furthermore, vaccination at day 1 is still possible in the presence of maternal antibodies, although interference may slightly reduce the immune response (Meulemans, 1988; Russel et al., 1995). If maternal antibody titers are high, passive protection is provided for at least the first 3 wk of life, and vaccination can occur after this period (Van Eck, 1990). In low-risk areas, protocols based on an initial vaccination at 3–4 wk after hatching are suitable if an inactivated vaccine is used for breeders.

In conclusion, our breeding flock of houbara bustards was effectively immunized against NDV by using an inactivated oil emulsion vaccine, injected SC, with a booster dose before each laying period. This vaccine protocol results in a higher level of NDV maternal antibodies in eggs and likely in day-old chicks. An effective NDV vaccine program and related biosecurity are essential components for NDV control and the subsequent success of houbara bustard breeding programs.


   ACKNOWLEDGMENTS
 
We thank His Highness Sheikh Zayed Bin Sultan Al Nahyan, Founder and Sponsor and His Highness Sheikh Mohamed Bin Zayed Al Nahyan, for his supervision and guidance. We also thank our colleagues in ECWP.


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
ALEXANDER, D. J. 2003. Newcastle disease and other avian Paramyxoviridae infections. In Diseases of poultry. 11th Edition, Y. M. Saif (ed.). CV Mosby Co.-Wolfe, Ames, Iowa, pp. 541–569.

———. 2000. Newcastle disease and other avian paramyxoviruses. In Revue Scientifique et Technique de l’OIE, pp. 443–462.

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Received for publication 24 September 2004.




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